Virus disease pandemics and epidemics that occur in the world’s staple food crops pose a major threat to global food security, especially in developing countries with tropical or subtropical climates. Moreover, this threat is escalating rapidly due to increasing difficulties in controlling virus diseases as climate change accelerates and the need to feed the burgeoning global population escalates. One of the main causes of these pandemics and epidemics is the introduction to a new continent of food crops domesticated elsewhere, and their subsequent invasion by damaging virus diseases they never encountered before.
Virus disease epidemics and pandemics threaten all types of cultivated plants including those grown to feed the world’s human population and its domestic animals, and others grown for ornamental, fiber or medicinal uses [1][2][3][4][5][6][7][34][35][36][1–7]. Virus epidemics also threaten wild plant communities growing in natural ecosystems [8][9][10][11][12][13][8–13]. With crop plants, they diminish the growth and vigor of infected plants, decrease gross yields and disfigure plant produce. The losses they cause vary from total crop failure to smaller scale, occur worldwide and have an estimated economic global impact of >US$30 billion annually [14][15][16][17][18][1,2,6,7,14–18]. They occur in all types of crop plants. These include staple food crops of crucial significance for achieving food security in subtropical and tropical regions [19][20][21][22][23][24][25][1,4,5,7,19–25]. With mixed species-managed pastures and wild plant communities in natural ecosystems, their detrimental effects on the growth and vigor of infected plants alter plant species composition. In managed pastures, they diminish the proportion of pasture plants versus weeds causing pasture deterioration and an inadequate feed base for livestock [26][27][28][29][30][31][32][33][26–33]. In wild plant communities, they alter the species balance and decrease species diversity, which damages ecosystems and can cause genetic erosion potentially leading to species extinction [34][35][36][37][12,13,34–37].
Development of damaging virus epidemics is favored by the introduction of new crops to parts of the world where they have never been grown before and the adoption of intensive cropping systems both of which lead to new encounters with virulent viruses infecting crops or indigenous vegetation. They are also favored by introduction of vulnerable new cultivars bred for increased yields [38][39][40] [1,2,4,19,20,38–40]. In mixed species-managed pastures, damaging virus epidemics are favored by factors such as relative grazing pressure and trampling by domestic animals resulting in increased insect vector numbers and virus spread by vectors or contact transmission [31][32][33][31–33]. In wild plant communities, they are aggravated by factors such as fragmentation into small patches of vegetation enclosed by crops or urban areas, livestock grazing and human disturbance, e.g., woodcutting and flower collection [41][4,9,10,37,41].
Several of the world’s plant virus disease pandemics and major epidemics have resulted from infection with emerging viruses that arose from new encounter situations in which indigenous viruses spread by spillover ( = host species jumps) from infected indigenous plants to infect introduced cultivated plants [42][1,4,5,7,19,20,42]. However, epidemics can also take place when introduced viruses spread to indigenous plants from infected introduced cultivated plants [4,9–13,37]. Thus, on the one hand, when introduced cultivated plants domesticated elsewhere grow next to indigenous wild plants or locally domesticated crop plants they never encountered previously, indigenous viruses associated with these indigenous hosts can spillover to the introduced crop plants causing virus disease epidemics in them. On the other hand, introduced viruses can also spread to indigenous crop or wild plants from infected introduced cultivated plants or associated weeds, causing virus epidemics. Both types of invasions require virus spread to occur at the interface between indigenous and introduced plants [43][44][1,4,9–13,37,40–44].
Pandemics or epidemics occurring in diverse crops and all continents, apart from Antarctica, were documented in a series of reviews written by the late Professor Michael Thresh [45]. These reviews covered the period from the inception of plant virology in the early 1900s up to 2006 [46][47][48][49][50][1,2,19,20,38,40,46–50]. In 1980, Thresh [1] provided a review of the origins and epidemiology of a wide range of important plant virus diseases. More up-to-date accounts of damaging pandemics or major epidemics involving several mostly single virus–host–vector pathosystems were described in several recent reviews [51][52][53][54][55][56][57][58][51–58]. In addition, a recent review focused on the global dimensions of plant virus disease [7].
This review describes virus disease pandemics and major epidemics that arose from spillover scenarios involving new encounters between indigenous viruses and introduced crops, rather than virus spread from introduced crops to indigenous crops or natural vegetation. It does this by providing historical and up-to-date information on five examples of virus diseases that threaten staple food crops critically important for food security in developing countries, placing special emphasis on the situation in sub-Saharan Africa (SSA). The sixth virus disease example threatens livelihoods in SSA because it devastates production of a valuable food export crop. In addition, brief coverage is provided of several other examples of major virus disease epidemics that arose from new encounters between indigenous viruses and introduced crops important for food security in different parts of the world.
In his 1970 review of ‘catastrophic plant diseases’, Klinkowski [59] [59] emphasized that many plant disease agents, including viruses, cause epidemics and pandemics, especially when they spread from their centers of origin into continents where they were formerly absent. He defined an epidemic as being “where a disease is spread over an area in which its causal agent has been present for a long time”; a progressive epidemic as “where it expands from this area into others”; and a pandemic as “where epidemics cause mass infections spread over several continents”. He gave five plant virus disease examples: sugarcane mosaic disease spreading worldwide fitted his ‘pandemic’ definition; plum pox, sugar beet yellows and tobacco veinal necrosis diseases spreading mostly in Europe matched his progressive epidemic definition; and cocoa swollen shoot disease (CSSD) spreading in Ghana, West Africa matched his epidemic definition. Subsequently, in plant virology, the term progressive epidemic has fallen into disuse and a plant virus disease pandemic has come to include “an epidemic occurring over a very wide area, crossing international boundaries and causing severe crop losses” [23]. In practice, however, the term epidemic is now widely used to cover all three of these types of epidemic situations, while the term pandemic has become restricted mainly to damaging virus diseases that spread widely between different countries in SSA, e.g., CSSD [18] and cassava mosaic disease (CMD) [23] and cassava brown streak disease (CBSD) [52]. In this review, the ‘pandemic’ definition now mainly used in Africa is also applied to other continents, otherwise the term ‘epidemic’ is used.
An emerging virus is usually considered to be “one that causes damaging epidemics but has only evolved or been recognized recently, changed its pathogenesis, increased its host range or increased its geographical distribution” [3,55]. Further, a re-emerging virus is usually considered to be “one that once caused serious disease problems, but then declined in importance before suddenly increasing in incidence and geographical distribution causing considerable crop damage” [4]. Therefore, the term virus emergence refers to “the first appearance of a virus and its associated initial increase in incidence/geographic range”, and the term virus re-emergence refers to “the reappearance of virus and its associated increase in incidence/geographic range”. When the term vulnerable is applied to a crop cultivar [20], this means that “the cultivar is both susceptible to virus infection (i.e., it becomes infected readily), and sensitive to infection once systemic infection has occurred (i.e., it develops severe symptoms)” [60][1,60]. Thus, susceptible is the opposite of resistance and sensitive is the opposite of tolerance [60]. The term virus spillover refers to “spread of a virus from naturally-infected host to a new host it has not encountered previously”, and the term spillback refers to “spread of a virus from the new host back to the natural host” [42].
Selection of local land races of crop plants from wild ancestors commenced more than 10,000 years ago in the worlds’ plant domestication centers [61][62][61,62]. Viruses from these wild ancestors were present among the land races derived from them and these indigenous viruses adapted to their new situation multiplying in cultivated plants growing mostly in mixed species cultivation [1,4,9]. Later, through international trade, crop plants were moved progressively away from their domestication centers to distant continents where they were often grown as monocultures. For example, the Columbian Exchange was responsible for the introduction of crops critical for food security to other continents following the Spanish 1492 arrival in the Americas, such as maize (Zea mays), cassava (Manihot esculenta), potato (Solanum tuberosum) and tomato (Solanum lycopersicum) [63]. In consequence, new encounters between introduced cultivated plants, and infected wild or crop plants occurred resulting in spillover of indigenous viruses into introduced crops. Sometimes epidemics arose soon afterwards and sometimes only after a considerable delay triggered by other factors, and some later became pandemics [1,4,9,18–23,40,52].
Successful spillover starts with spread of already existing genetic virus variants from a virus infection source plant to the new host plant, and the outcome for each individual variant depends on its relative abilities (i.e., fitness) to survive once it infects each host, adapt to new hosts or vectors and achieve efficient epidemic spread [64]. A range of factors favor successful virus spillover, emergence or re-emergence. These include: presence of efficient indigenous or introduced virus vectors, including “supervectors”; introduction of vulnerable crop cultivars; adoption of cultural practices involving agricultural intensification, extensification and diversification; intensive wildflower production and conservation projects; the relative ability of a virus to generate virulent new variants through mutation, reassortment and recombination; and climate change arising from global warming [1,2,4,16,19,20,42,55,64–73].
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